SUCCESSIONAL BrODIVERSJTY IN INSECT SPECIES ON BURIED CARIUON

" - IN THE VANCOUVER AND CARIB00 REGIONS

B Sc Simon Fraser university 1994

THESIS SUBMITTED IN PARTIAL FULFILLMENT OF

Y

THE REQUIREMENTS FOR THE DEGREE OF w

I

MASTER OF PEST MANAGEhlENT

Z

+ in the Department

Biological Sciences

O Sherah Lymette Vwaerhoven, 1997

SIMON FRASER UNIVERSITY

April 1997 L

J

" All rights reserved This work may not be

reproduced in whole or in part, by photocopy

or other means, without permission of the author

National Library 1*1. of Canada Bibliotheque nationale du Canada

Acquisitions and Acquisitions et Bibliographc Services services bibliograph~ques

,' 395 Wellington Street 395, rue Wellington

' OnawaON KlAON4 OttawaON KlAON4 Canada CaMda

8% *. r

= ..

The author has granted a non- exclusive licence allowing the National Library of Canada to reproduce, loan, dstribute or sell copies of h s thesis in microform, paper or electronic formats. q

! The author retains ownership of the copyright in this thesis. Neither the thesis nor substantial extracts from it may be printed or otherwise reproduced without the author's permission.

+ Your h*, Votre refermce

Our hle Norrf reference

A.

L'auteur a accorde une licence non exclu$ve pennettant a la Bibliotheque nationale du Canada de reproduire; p&er, hstribuer ou vendre des copies de cette these sous la forme de microfiche/filrn, de reproduction sur papier ou sur format electronique. ,

f 1 L'auteur conserve la propnete du -8

droit d'auteur qui'protke cette these. Ni la these ni des extraits substantiels de celle-ci ne doivent itre imprimes ou autrement reproduits sans son autorisation.

g. .;

APPROVAL

Name: Sherah Lyrmette Van Laerhoven

4

Degree: a

Master of Pest Management

Titleof Thesis:

SUCCESSIONAL BIBDIVERSITY IN INSECT SPECIES ON BURIED CARRION IN THE VANCOUVER AXD CARIB00 REGIONS OF BRiTISH COLUMBIA

Examining Committee:

Chair: Dr. R . Brooke, Associate Professor

-- - + W ' . - ,Dr. G. S. ~ n d e r k n , ~;s:stant Professor. Senior Supem~sor

Department of Biological Sciences. SFCi

- - -

Dr. J \ H. Borden, Professor Department of Biological. Sciences, SFL

, J I/ - '

n, Assmiate Professor rce/Environmental Management, SFV

- .- - ~ t a # ~ ~ t . Robert staffr Royal Canadian Mounted Police (Retired)

/' - i ' Dr. D. Glllespie, Research Scientist

Agriculture and Agn-Fwd Canada Public Exarmner

Date Approved:

ABSTRACT

I established a database of insect succession on buried c h o n in two

biogeocllmatic zones of British Columbia over a 16 month period bepnning June

1995 Pig (Sus xrofa L ) w c a s e s were buried immediately after death, buried 48 h

after death and buned then subsequently disturbed, in the Coastal Western Hemlock

and Sub-boreal Spruce biogeociirnatic zones of British Columbia Buried pigs

exhibited a distinct pattern of insect diversity, relative abundance and succession from

that whch occurred on hve-ground carrion Insect communities on buried camon

exhibited greater species nchness and evenness compared with above-ground carrion

The species composition and time of coloniation for particular species differed

between the two zones Therefore ideally, a database of insect succession on buried

carrion should be established for each major biogeoclimatic zone I did not observe d?

maggot masses on any of the buned carcasses, therefore the presence of maggot

masses may indicate a delayed burid Soil temperature was a better indicator of .

~niemal buned carcass temperature (r2=0 92, P 0 0001) than was ambient air

temperature (r2=0 60. PC0 0001 ). thus soil temperature should be used to determine

developmental rates of insects for determination of the post-mortem interval by a

formsic entomolo_~lst

To Gail , /Joh and Dave -

for always believing in me.

Poor soul, the centre of my sinful earth, these rebel powers that thee array;

Why dost thou pine within and suffer death, Painting thy outward wdfls so~costly gay?

Why so large cost, having so short a lease, Dmt thou upon thy f&ng mansion spend?

Shall worms, inheritors of this excess, Eat up thy charge? is this thy bdy's end?

Then soul, live thou upon thy servant's loss, And let that pine to aggravate thy store;

Buy terms divine in selling hours of dross; Within be fed, without be rich no more:

So shalt thou feed on Death, that feeds on men, And Death once dead, there's no more dying then.

W'illiam Shakespeare, Sonnet .I 46

ACKNOWLEDGEMENTS

This research was supported by the Canadian Police Research Centre,

especially Sgt. Ken Beiko and Mr. Nick Cartwright. 1 would like to thank the

Malcolm-Knapp Research Forest and the Alex Fraser Research Forest staff for their - hnd coo.peration; all the high school and undergraduate volunteers, fhends and

collegues who spent many hours diggmg graves, placing carcasses, collecting pitfall

traps and sorting through soil, G St I-hlaire for his assistance placing carcasses,

- Anderson lab-mates for assistance throughout the research, Simon Fraser University

for the use of its facilities, Dr T Finlayson, Dr H R MacCarthy and the International

Association for Identification for their generous scholarshp endowments, the National

Identification Service, in particular J Poirier, E C Becker, A Davies, A Smetana, Y

e

Bousquet, L LeSage and J Derus for all the hours they spent identifjmg some of my

spectmens, my Friends, family and colleapes who supported me and made ths degree

far more enpvable. my supemsory committee, Dr d 'borden, Dr K Lertzman and % "

Staff' Seryeant R Stair (Retired) for their support and gu~dance, and especially Dr - . , ?

Gad Anderson, for constant support. guidance and hendsfip W~thout her, thrs

degree would not hate been possible

TABLE OF CONTENTS

TITLE 'PAGE I

11 I

APPROVAL PAGE . . I I

. . . ABSTRACT 111

i

DEDICATION iv

QUOTATION v

6:

ACKNOWLEDGEMENTS vi

TABLE OF CONTENTS vii / I-

LIST d~ TABLES ix d s

LIS? OF-FIGURES x fi-

1. INTRODUCTION 1

1 .1 0B.JECTIVES 1.2 RESEARCH AREAS 1.3 EXPFRIMENTAL PROTOCOL

-1 3 1 Expenmental Carcasses 1 3 2 C W z o n e 1 3 3 SBS zone 1 3 4 Temperature and B~omass Loss Measurements

1.4 SAMPLING METHODS 1 4 1 Data Record~ng 1 4 2 On-S~te Collect~on 1 4 3 F~eld Morgue Collection

1.5 QUANTITATIVE ANALYSES

2.1 TEMPERATURE 2.2 DECOMPOSITION RATE

2 2 1 Fresh Stage 2 2 2 Bloat Stage 2 2 3 Act~ve Decay

2.2 4 Advanced Decay Stage 2,2.5 DrylRemains Stage

2.3 BIOMASS LOSS 2.4 INSECT D M R S I T Y 2.5 INSECT SUCCESSION

2.5? 1 Immediate burial vs. above-ground 2.5.2 Immediate vs. delayed burial 2.5.3 Immediate vs. disturbed burial

* 3. DISCUSSION 40

3.1 DIVERSITY IN EPHEMERirL HABITATS 3.2 SUCCESSION

3 2 1 irgmedia&ly buried carcasses *

3 2 1 1 Dipteran canion fauna 3 2 1 2 Coleopteran carrion fauna 3 2 1 3 Hymenopteran carrion fauna

3 2 2 Carcasses buried after 48 hours . - 3 2 3 Disturbed budal .'

3.3 Ecological Roles of Carrion Fauna 3.4 FORENSIC IMPLICATIONS

3 4 1 Hapied Time Since Death I

a 3 4 2 Temperature =s.

.- 3 4 3 Indicator species ' 3 4 3 1 Fapily,Calliphoridae 3 4 3 2 Family Muscidae

* r e 3 4 3 3 Family Fanniidae

3 4 3 4 Family ~horidae 3 4 3 5 E;&nily Sphaeroceridae 3 4 3 6 Family Heleomyzidae

a. 3 4 $7 Coleopteran Families 3 4 4 Recommendations

- viii

LIST OF TABLES r

Table 1. Linear regression analysis of temperature data collected during d decgmposition of pig carcasses in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) bibgeoclimatic zones of British Columbia, June 1995 to October 1996 .. 43% 17

. . . ._ . Table 2. Decompositional stages of pig carcasses buried immediately, buried 48 h

, ~ after death, buried then disturbed and left above ground in-the Coastal Western .. Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic zones of British

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Columbia.. 19?,

Table 3. Simpson's index of diversity, comparing the relative abundance of each insect species collected on pig carcasses afler death, in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic zones of British Columbia An index of one indicates a highly diverse community, while an index of zero , indicates a community with no diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ' 2 5

Table 4. Succession of insect species collected through exhumation (Ex) and pitfall traps (Pt) on buried and above-ground pig carcasses in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeockmatic zones of British Columbia A = adults, P = pupae, PC = pupal cases, L = larvae, E = eggs, - = no collection possible t 3 1

LIST OF FIGURES

Figure 1. Mean daily internal temperature of above-ground and buried pig carcasses measured every 90 min in the Coastal Western Hemlock (CWH) g d in the Sub- boreal Spruce (SBS) biogeoclimatic zones of British Columbia Ambient air temperature in the CWH zone was recorded twice daily from the Malcolm-Knapp Research Forest weather station: 2 km from the research site Ambient air temperature in the SBS zone was measured every 90 rnin at'the research site 12 .

-, Figure 2. Mean daily intkrnal buried pig carcass temperature in the Coastal Western

Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic zones of British Columbia (estimated by gra,ve temperature in the CWH zone) measured every 90

b min fiom November 1995 (1 59 days since death) to October 1996 Ambient air temperature in the CWH zone was recorded twice daily from the Malcolm-Knapp

t Research Fmest weather station, 2 km from the research site Ambient air temperature in the SBS zone was measured every 90 min at the research site 13

- Figure 3. Mean daily ambient air temperature, ambient grave temperature and internal *

buried pig carcass temperature measured every 90 min for the first 90 days after death in the Sub-boreal Spruce (SBS) biogeoclimatic zone of British Columbia Day 0 = 10 June 1995 14

Figbe 4. Maximum and minimum ambient air temperatures recorded twice daily fiom the Malcolm-Knapp Research Forest weather station and maximum and minimum internal buried pig carcass temperatures measured every 90 min for the first 90 days after eath in the Coastal Western Hemlock (CWH) biogeoclimatic zone,

* British Co 1 umbia Day 0 = 17 June 1995 , 15

Figure 5. Percent weight loss during decomposition, in above-ground and immediately buried pig carcasses in the Coastal Western Hemlock (CWH) and Su

carcasses taken fiom Dillon and Anderson (1995) Spruce (SBS) biogeoclimatic zones of British Columbia Data. fiom

22

Figure 6. Species abundance (dominance) compared with species richness (diversity) plots of insect communities on pig carcasses in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic zones of British Columbia 2 3

Figure 7. Relative abundance (ranked in order of increasing diversity from left to right) of the five most abundant species within four communities of insects collected from pig carcasses in the Coastal Western Hemlock (CWH) and Sub- boreal Spruce (SBS) biogeoclimatic zones of British Columbia 2 6

b - Figure 8. Species richness (within order and family) of insect communities~collected - from pig carcasses b u k d immediately and pig carcasses above grou~ld in the Coastal wedern Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic . ' zones of British Columbia.. . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ' . . ( . . . . . . . 27

Figure 9. Average linkage clustering of insect cornmunitles, based on the presence and absence of species collected fiom carcasses in the Coastal Western Hemlock (CWH) and Sub-boreal Spruc&SBS) biogeoclimatic zones of British &

Columbia 2 9

Decomposing bodies constitute a rapidly changing habitat AAer death, carrion 1

'

undergo rapid physical, chemical and biologwil changes during the decomposition

process At each stage of decomposition, carrion is attractive to different species of b

insects These insects colonize the remains in a predictable sequence, so that an

analysis of the arthropods on a human homicide victim, weeks or months after death,

can lead to an accurate estimate of elapsed time sincedeath Ths information may be . -

vital in a homicide investigation (Anderson and VanLaerhoven 1996)

The succession of instxt species on camon varies according to temperature,

habitat and geographic location (Reed 1958, Payne 1965, Demo and Cothran 1976,

Goddard and Lago 1985, Greenberg 1985, Goff el a1 1986, Goff and Odom 1 987, , , Goff r f a/ 1988, Goff 199 1, Goff and FIynn 199 1 , Anderson and VanLaerhoven

1996) T k variation occurs on both above-ground and buried carcasses,(Rodriguez

and Bass 1985, Smith 1986), but the fomtkm of the remains influences the time

requlred for insects to locate a carcass. the sequence of colonization and the rare &

decomposition (Payne el a/ 1968, Rodriguez and Bass 1985, Smith 1986) This

vanation makes extrapolation of insect succession databases between habitats and

geographc locations extremely difficult However, it is hypothesized that once insects .

locate buried remains, they will feed and develop normally, and will colonize in a

predictable sequence

No experimental research into insect succession on buried corpses hasbeen

done in Canada In fact, there has been no publishedexperimental research on insect

succession on buried corpses which accurately mimics a homicide scenario anywhere

in the world

l . 1 OBJECTIVES

Ths research was designed to mimic three homicide scenarios accurately

/

immediate burial, delayed burial (many perpetrators do not dispose of the body

immediately), and disturbed burial (perpetrators often return to and disturb the site of

a forensic burial)

The specific objectives were B

" X . to examine the successional biodiversity in insect species on immediately buried . .~

F- 3:

,.-&A .. . . -.

carrion in two biogeoclimatic zones, the Coastal Western Hemlock (CWH) and

Sub-boreal ~ ~ r u & (SBS) ?on*es of British Columbia (Meidinger and kojar 199 1 ).

to determine the effect of delayed burial on the successional biodiversity of insect

species on buried carrion,

to determine the effect of.disturbance on the successional biodiversity of insect

species on buried carrion, and

to establish a database of insect succession on buried carrion in both the CNW and

SBS zones (characteristic of the Vancouver mdCariboo Regons, respectively) of

British Columbia for use in homicide investigations

dl Z

1.2 RESEARCH AREAS

Experimental areas were located in the CWH zone within the Vancouver

Forest Region and the SBS zone within the Cariboo Forest Regon. Most of the

research was concentrated in the CWH zone since most buried corpses are found there

(Anderson 1995) Only immediately buried and disturbed carcasses %ere studied in

the SBS zone in conjunction with extensive exposed carcass experiments conducted at

the same time (Dillon 1997). The research areas were located in the University of

British Columbia's (U B C ) Alex Fraser Research Forest, Gavin Lake Block just east

of Williams Lake in the Cariboo Forest Region and in U.B C 's Malcolm-Knapp

Research Forest in Maple h d g e in the Vancouver Forest Region, where above-ground : . +

carcass experiments had been conducted in 1994 (Dillon and Anderson 1995) Both * .

areas were chosen 041 the basis of representative soil type and vegetation

Two weeks before carcass placement, 250 mL glass jar pitfall traps containing

soapy water were placed at each planned carcass site and atthree contr9l~sites (no . .

carcass), at least 15 m fiom.the carcass sites After burial, the pitfall traps were placed

in the soil above the carcasses to trap a sample of the insects attracted to or leaving the

remains The control pitfall traps remained at their original sites

At each site graves were dug with a shovel on the same day, deep enough to

allow the upper surface of a carcass to lie approximately 30 cm below the forest floor

All graves were at least 15 m away from the next grave or above-ground carcass, so

that olfactory orientation of insects to each carcass was minimally influenced

4 - -

1.3 EXPERIMENTAL PROTOCOL ' a

1 . X I Experimental Carcasses

Twenty-three kg (50 Ib) pigs (Sus scrofa L ) were used as surrogate human

models, as these are considered to be excellent models for human decomposition

(Catts and Goff 1992) A 15 cm pin gun shot to the head was used to lull all the pigs

To allow insertion of temperature probes, the carcasses were shot second t'ime, in

the side of the thorax using a 22 caliber rimfire bullet This produced a small entrance -

wound just wide enough tc allow insertion of the probe, b~ did not produce an exlt L'

r II

wound Because clothing influences insect succession (Dillon and Anderson 1995)

and most homicide victims are clothed or have cloth associated with the body L

(Anderson pers com ), each carcass was identically clothed with underwear, a T-

shirt, blouse, shorts and socks For immediate and disturbed burial treatmen6 a -

freshly killed pig was placed in eachgrave wittun hours of deathand the grave was

filled to ground level with loosely packed soil The top of each grave was disguised

with branches, leaves and rocks Pigs in delayed burid treatments were identically

buried 48 h after death Above-ground carcasses were protected from large scavenger

attack by wire mesh (4"x2", 12 5 gauge) staked to the ground over the entire carcass

Buried carcasses were protected by wire mesh staked down over the grave

1.3.2 CW H zone

On 17 June 1995, 15 pigs were buried immediately after death (wittun 5 h of

death) Three of these pigs were exhumed at each of 2 and 6 weeks and 3, I I and 16

months after death Nine pigs were buried 48 h after death Three of these pigs wefe

exhumed at 2 and 6 weeks, and 3 months after death Three control pigs were left

above ground and were examined at the same \

- 1.3.3 SBS zone .

On I0 June 1995, 12 pigs were buned

time as the exhumed pigs

immediately after death (uithin 8 h of

death) Three of these pigs uete exhumed at each of 2 and 6 weeks. and 3 and 16

months after death Three pigs exhumed at 2 weeks after death, were re-buned after

sampling to detemne the effect of d~sturbance They weTe a g m exhumed at 6 weeks

after death and compared u ~ t h the three pigs exhumed for the first tme at 6 weeks

after death Three control carcasses were left abo~ve ground and were e v m n e d at 2

u eeks after death The? se re then consumed b) a large scab enge: and could not be

sampled agam

1.3.4 Temperature and Biomass Loss %leasuremeats

Internal carcass trmpsrantre w a s taken From one abbe-pound carcass and

one buned carcass f the last to be exhumed1 u~ttun each bro_aemlirnat~c zone .hb ien t

a r and sod temperarurc (fiorn soil adjacent to the buned carcass) uas recorded in b a t h

zones Temperatures heye recorded using tuo ppcs of dataloggers Double channel

datalo@& (~rnart~eader'l', Young Environmental Systems, kchmond, B C )

measured the temperature every 30 rnin Single channel dataloggers (~obo ' , Hoskins -.

\

Scientific, Vancouver, B C ) measured the temperature e v e j 9 0 minutes Failure of

i

all but one kobo' and several ~mart~eaders" precluded recording of additional

internal carcass, ambient air or soil temperatufes Ambient air temperature data in the

CWH zone ae;e lost due to these failurgs, thus ambient air temperature data were

taken fiom an Environhent Canada weather station in the Malcolm-Knapp Research

IL Forest, 2 h south of the research siie

Biomass loss was measured by placing an exhumed carcass on a mesh platform

and weighmg it using a 70 kg ( 1 50 lb) scale on a pulley system Above-ground w

carcasses were not weighed, because the disturbance could have affected the

succession pattern since the carcasses were not on mesh platforms i

'+ . f.4 SAMPUNG METHODS

At each sampling date, insects in each pitfall trap were separated fiom the

soapy water by the use of a small tea strainer and placed in 70% ethanol in a sterile

100 rnL vial Fresh soapy water was then placed in each pitfall trap Insect species

that were collected in equal abundance fiom control and carcass sites were excluded P

because these were considered to be endemic species that are not associated wlth

The buried carcasses were exhumed carefully, in the manner of crime scene

investigations and examined for insect+ The exhumation consisted of three

components data recording, on-site collection and field morgue collection When

insects were sampled, 10-20 individuals per species were routinely collected All . - w

individuals of less numerous species were also collected'

1.4.1 Data Recording

Extensive photographic records during all stages of exhumation were

supplemented by written notes of all observations These were made with reference to

a Ix 1 m gnd, with four 50 cm2 quadrats, laid out before the excavation

1.4.2 On-Site Collection

Collection of insects began with carehl removal of surface plants They and

the exposed ground were examined visually for insects Next, soil was removed

systematically, one quadrat at a time moving from the outermost to the innermost area

(Skinner and Lazenby 1983) Soil y hand and visually inspected for .

0

insects, samples of which were collected When the entire corpse was exposed,

photographs were taken and notes made, then the carcass was lifted out of thegave

and moved away on a mesh platform Soil in the bottom of the grave was examined

visually and samples of all insect species were collected

1.4.3 Field Morgue Collection

-. The entire exhumed carcass, as well as all areas of the clothing. including

pockets, were examined and sampled for insects using forceps or gloved fingers The

carcass was then placed in a plastic bag and later disposed of by incineration Half of

the larval Diptera were preserved in 70% ethanol in screw cap vials, while the rest

were kept alive in sterile 250 mL vials containing some beef liver or pork with a paper

towel lid affixed by an elastic band These were reared to adulthood in the laborator)-..

facilitating identfication Adult insects were pinned and larval insects were labeled and

preserved in 70% ethanol for later identification

All larval Calliphoridae and Muscidae were examined under a binocular

microscope to determine instar by number of spiracular slits (Srmth 1986) Insects

were identified using keys and comparisons with verified specimens in the Srmon

Fraser University forensic insect reference collection Specimens that were d~fficult to

identify were sent to the National Identification Service in Ottawa for identrfication

and to provide voucher specimens for our reference collection

Above-ground control carcasses were sampled in a similar manner on each

exhumation day, but on a lesser scale because above-ground successron can be

determined From the established database (Dillon 1997)

1.5 QUANTITATIVE ANALYSES

Only insects collected fiom the grave soil or on the carcasses were used in the

quantitative analyses Therefore insects collected in pitfall traps were only used in the

succession table Simpson's index of diversity ( I -D) (Krebs l989), defined as 1 - (the

probability of picking two organisms that are the same species) or

where p, = the proportion of individuals of species i in the community, was calculated

usmg the relative abundance of each species within the different treatments Ths

index gives a measure of diversity of insect species, in whch a score approachng 1

indicates hgh diversity

I compared the similarity or difference in species composition between .... .

. ..

, treatments using average linkage clustering (Minitab 1994) Treatments that are most

similar in species composition have the highest scores and are clumped closest

together in the cladogram A score of 100 means that the two treatments being

compared had identical species compositions Using average linkage c1ustering:the

distance between two clusters (or treatments) is the mean distance between a vanable

(species a) in one cluster and the same variable In the other cluster (Minitab 1993)

Therefore, two treatments composed of identical species will have no distance

between them on the cladogram and will have a similaritj. of 100 The distance matnx

(d,) is calculated by

* where NL, N,, N, = the number of variables in the clusters k, 1 and m

The correlation distance is dculated by

where p,, = the Pearson product moment correlation between variables i and j

I used Microsof3 Excel (Mcrosofl 1985) to calculate the linear regression

equations predicting internal carcass temperature from ambient air temperature and

soil temperature and predicting soil temperature From ambient air temperature The

temperature data for the first three days after death were omtted to eliminate the

effect of algor Morm

2. RESULTS

ES 2.1 TEMPERATURE

Differences were observed between the ambient air and grave soil temperatures

and between the internal carcass temperatures of buried and above-ground pigs

These trends held true for carcasses in both study sites. In both zones, buried carcasses

did not show the same internal temperature spike experienced by above-ground,

carcasses (Figure 1 ) During the winter months in the SBS zone, internal buried

carcass temperature did not fluctuate with ambient air temperature (Figure 2)

However, during the winter months in the CWH zone, the internal buried cpcass

temperature (estimated by grave temperature' because the datalogger failed) did

fluctuate significantly (r2 = 0 73, P < 0 0001) with the ambient air temperature

recorded at the Malcolm-Knapp ~ese'arch Forest weather station (Figure 2) t

There was less fluctuation in soil than in ambient air temperature overall, as

illustrated by data collected in the SBS zone (Figure 3 ) AAer a l p r mortis was

complete, there was little difference between grave temperature and internal carcass

temperature In both zones, diurnal fluctuations were much greater in the ambient air

temperature, than in the internal buried carca~s temperature, as illustrated by data

collected in the CWH zone (Figure 4)

The ux of g m e temperature 1s justlfkd b! the strong relationsh~p bemeen internal carcass and gra) e tem@mtures recordedior 262 days from the SBS zone (?=o 92. P <O 000 1 )

Figure 1. Mean daily internal temperature of above-ground and buried pig carcasses measured every 90 rnin in the Coastal Western Hemlock (CWH) and in the Sub-boreal Spruce (SBS) biogeoclimatic zones of British Cohmbia Ambient air temperature in the CWH zone was recorded twice daily from the Malcolm- Knapp Research Forest weather station, 2 krn from the research site Ambient air temperature in the SBS zone was measured every 90 min at the research site

C W H Zone Day 0 = E 7 June 1995

35 -

Pig d i e n large I .

30 ; ' I C

I , sea\ engcr

SBS Zone Day 0 = I0 June i 995

o * - - + . * . -

0 10 2 0 3 0 4 0 50 60 7 0 8 0 <I(

Elapsed T i m e Since Death in Days

Buried pig - - - Ambient Air - - . - - . Above ground p ~ g 1 '

Figure 2. Mean daily internal buried pig carcass temperature in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeociimatic zones of British Columbia (estimated by grave temperature in the CWH zone) measured every 90 rnin from November 1995 (1 59 days since death) to October 1996 Ambient air temperature in the CWH zone was recorded twice daily frbm the MalColm- Knapp Research Forest weather station, 2 km away from the research site Ambient air temperature in the SBS zone was measured every 90 kin .at the research site

C W H Zone Day 159 = -23 November 1995

I 3 0 - . A

15 - W~nter - ground frozen

SBS Zone Day 1 59 = 16 November 1 995

! Elapsed Time Since Death -in Days

Buried pig - - - Ambient Pur 13

Figure 3. Mean daily ambient air temperature, ambient grave temperature and internal buried pigcarcass temperature measured every 90 min for the first 90 days after death in the Sub-boreal Spruce (SBS) biogeociimatic zone of British Columbh. Day 0 = 10 June 1995. .

- - - Grave 30 -

- - - - - . Ambient h r

Buried pig

b

0 . - * + * - - * * - ~ + - * - - .

0 L 10 2 0 3 0 40 50 60 70 80 , 90

Elapsed Time Since Death in Days

Figure 4. ~ a x i ~ m and minimum ambient air temperatures recorded tHlce daily 1

From the Malcolm-Knapp Research Forest weather station and maximum and minimum internal buried pig carcass temperatures measured every 90 rnin for, the first 90 days after death in the Coastal Western Hemlock (CWH) biogeoclimatic zone, British Columbia Day 0 =, 1-7 June 1995

Buried Pig

Ambient Air

* .

0 10 2 0 30 40 50 60 70 8 0 90 %

Elapsed Time Since Death in Days

& Weather station ambient air'temperature was not a good predictor of the

internal temperature of above-ground carcasses in the CWH zone, although it was a

good predictor of the internal temperature ofiabove-ground carcasses in the SBS zone

\ before the action of the maggot masses increased the internal temperature (Table 1 )

- Soil e a t u r e was an excellenj predictor .- of internal buried carcass temperature in

the SBS zone (Table 1 ) Mean and minimum ambient air temperatures were also

acceptable predictors (r2 > 0 5) of internal buried carcass temperature in the SBS zone,

but only in the spring, summer and fall months (Table 1 ) In contrast, ambient air

temperature taken from a weather station 2 km away was not a good predictor (r2 <

0 5) of internal buried carcass temperature in the CWH zone, likely due to small - C

sample size, although it was an acceptable predictor of grave temperature (Table 1 )

2.2 DECOMPOSITION RA TE

The rate of decomposition of buried carcasses was considerably slower than

for the above-ground carcasses Although decomposition is continuous, Payne et a/.-

(1968) recognized five stages of physical decomposition. which I have adapted to

characterize the experimental carcasses

2.2.1 Fresh Stage

This stage began at death and continued until bloating okthe carcasses was

visible This stage was not observed after the initial placement of the carcasses since

- - - 0 c c 0 C 0 C O O

c C c C C C C 2. =:

0 I-J N

LI 3 3

- 3 0

d I-J 0 m c v. O O C

00 r? 00 GOC+ O C O

r ' l N

both above-ground carcasses and buried carcasses had passed beyond ttus stage bt

two weeks after death (Table 2)

2.2.2 Bloat Stage

By 2 weeks after death above-ground carcasses had passed the bloat stage

(Table 2 ) , characterized by the accumulation o f gases wittun the body as anaerobic P

bactena wthin the gut begin to digest the carcass Ths was ewdenced by the deflated

nature of the carcasses However, buried bodies decompose at a much slower rate.

aliowng charactenzat~on on the basis of disaniculation By 2 weeks after death.

burled carcasses had entered a primary bloat stage (Table 2 ) , charactenzed b) both

the bloated appearance and the lack of disart~culation By 6 weeks after death. bunsd

carcasses ue re in a secondary bloat stage (Table 2). still bloated. but w ~ t h the lmbs

2.2.3 A c t h e DecQ

Thrs stage Has charactenzed b) the deflat~on of the carcass and d l san~cu la !~~r !

a< ik head Flesh and s h n u e r e stdl present B) 2 weeks after death. the abo%c-

g.-wr.~:: ciflcases u t r e in t h s s a g e (Table 2) . kith large m a g o t masxi rapid!\

:.:1z3urnmz - ffeih The bun& carcasses *ere in thrs stage b? 3 months afier death

Table I \ o masgo? rnaj*j u e r e presenr The abdomen u a s c o l i a p s q u3:t :be

~ 3 . d EX! ; q ~ dia'tii~lald The carcasses ue re Len u e ~ ui th 2 strong d ~ ~ : OKC

.%

Table 2. Decompositional stages o f pig carcasses baried immediately, buried 48 h after death, buried then disturbed, and left above ground in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic zones of British Columbia

Tune taken to reach each stage of decornposrtion (days) Fresh Pnrnary Secondary Active Advanced Dry 1

Zone Treatment bloat bloat decay decay rema~ns P

CWH Immednte bunal 0 < 14 < 45 < 90 < 335 + 490 Delayed bunal 0 < 14 < 45 < 90 nta nla Above-ground 0 stage not observed < 14 < 45 < 90-

SBS Irnrndate bunal 0 < 14 < 45 < 90 < 490 + 490 Disturbed bunal 0 d a < 45 n/a n/a m'a Above-around 0 stage not observed < 14 n/a n/a

+.it :his point. most of the flesh had been removed, but slun, bone, fat and

;mii.+it;c imaned on above-ground carcasses, which had reached this stage by 6

&csk1 35sr dralh mthe CUH zone (Table 2) The above-ground carcasses in the SBS

r - x e had k e n eaten bj a large scavenger by this time By 11 months after death, the

+..r:d a c a s s e s tn the Ct+M zone had reached the equivalent of this stage (Table 2)

f-m~t4 flesh remained. although some of it had turned to adipocere tissue, formed by

~~~ :% SOE: erslon of soft tissue toRydrolyzed fat in the presence of cool moist soil or

~t arr r I Spl tz and Fisher I 973) and the abdomen had collapsed The carcasses were L

, < T C

j?:!i f a ~ r l y wet &I6 months after death, the buried carcasses in the CWH zone were - m!1 in this stage (Table 2), with the remaining flesh turned to adipocere tissue and the

. -.T _. . *.

nbcage collapsed, giving the carcasses a flattened appearance Buried carcasses in the

SBS zone had reached the advanced decay stage by the time the expenment was

terrmnated at 16 months after death (Table 2) They resembled the buned carcasses

exhumed in the CWH zone at I 1 months after death

2.2.5 Dry/Remains Stage

By 1 1 months after death, the above-ground carcasses had entered ahls final

f l

stage with only bone, cartilage and some skin remamng (Table 2 ) H I I S of clcrfhrng and

bones were the only remaining ewdence of these carcasses

2.3 BIOMASS LOSS

- Biomass loss in buried carcasses was slightly faster in the CWH zone than in

the SBS zone (Figure 5). However, buried carcasses in both zones lost biomass much

more slowly than above-ground carcasses in the shade in the spring of 1994 in the

CWH zone (Dillon and Anderson 1995) The slower rate of decomposition and

decreased rate of biomass loss lengthens insect succession on buried carcasses

2.4 INSECT DIVERSIN

Diversity of insect species consists of both the species richness and the relative

abundance of each species Examining the dominance-diversity plots (Krebs 1989)

(Figure 6) for aboue-ground carcasses in both the CWH and SBS zones, it is

lmmedlately apparenl that i h i k communities have low species richness compared ,+~th $9 d

that on buried carcasses, and are dominated by a few species of hi@ relative ;. <%

abundance Although it appears that the above-ground commun e SBS zone is

much less diverse than in the CWH zone, this was due to the small sample size since i

the carcasses were iemoved by a scavenger Therefore, all the later species of insects ..- /

that would have colonized these carcasses could not be included in the diversq , i

calculat~on Buned carcasses appear to have a more diverse communi$ than above- @

ground carcasses, with greater species richness and evenness qlthough ~t appears that

disturbed burial carcasses have less species richness, ths is'due to the much-smaller

sample size compared with the other buried carcasses There is no apparent d~fferenct.

Figure 6. Species abundance (dominance) compared with species richness (diversity) plots of insect communities on pig carcasses in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) b~~~eoclirnatic zones of British Columbia

CWH A bove-G round

CU'H Immediatei) Buried

S B S Above-Ground

SBS Immediately Buried

SBS ~crr" , D i s h t r b d Burial

Ranked Specws in Order of Abundance

2 7

in relative abundance of sdecies between the different burial treatments This is 1

confirmed by Simpson's index of diversity (Table 3 )

Examining the relative abundance of the five most abundant species in burial

and above-ground communities collected from carcasses (Figure 7), it is apparent that

the community on the above-ground carcasses in the SBS zone is dominated by one,

species. Phormra regma (Meigen) The other three communities e h b i t more

evenness, although the community on the above-ground carcasses in the CWH zone is

co-dominated by Phorrn~a regma and Ltrciha rll~rstr~s (Meigen)

All four communities are composed of insects fiom two orders Diptera and

Coleoptera (Figure 8) The species richness within different families fiom these orders

is higher in the two communities on buried carcasses, than in the two above-ground

carrion communities (Figure 8) Species richness is high in the family Staphylinidae

(Coleoptera) for all four communities However, in the two buried camon and in the

above-ground CWH communities, other coleopteran families also have relatively h g

species richness The same trend is true with the dipteran families The dipteran family

Calliphondae plays a dominant role in the' species richness of three communities. but

not in the immediately buried CWH community Unlike the two above-ground

communities, in the buried carrion communities. the family Muscidae is domijp'rit ?'1* , 4 .

There appears to be very little difference in the species richness of different families pe

between the CWH and SBS ~zones Although the SBS above-ground

Table 3. Simpson's index of diversity, comparing the relative abundance of each insect species collected on pig carcasses after death, in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biogeoclimatic zones of British Columbia An index approaching 1 indicates a highly diverse community, while an index of zero indicates a community with no diversity

Zone Treatment Simpson's index ( 1 -D)

SBS Above-ground 0 1

Buried Q 9 - Disturbed 0 9

CWH Above-ground 0 7

Buried

Delayed

Figure 7. Relative abundance (ranked in order of increasing diversity from left to right) of the five most abundant species within four communities of insects collected fiom pig carcasses in the Coastal Western Hemlock (CWH) and Sub- boreal Spruce (SBS) biogeoclimatic zones of British Columbia

CWH Above-ground

CWH Buned

unmdately

SBS Buned

m d a t e l y

community appears to have less species richness than the-other three communities,

thk is due to small sample size.

However, there is a difference in the species composition of the communities in

the CWH and SBS zones when the different communities are compared -using average

linkage clustering (Figure 9), based on the presence and absence of the different #

species collected during different sampling dates The communities in the SBS zone

are more similar to each other in species composition, than they are to the I

j

communities in the CWH zone and v ~ c r verso. Both treatment and time since death

appear to influence the degree.of simiSarity in species composition between different B'

communities Within the CWH zone, the communities of insects collected from

immediately and delayed buried carrion at 6 weeks after death are more similar to each

other than they are to the community collected fio'm above-ground carrion at 6 weeks

after death (Figure 9) It is interesting to note that CWH and SBS communities of

insects collected on above-ground carrion at 2 weeks after death were more similar to

each other than to any other community, likely due to the dominance of blowfly

species on these carcasses

2.5 INSECT SUCCESSION

2.5.1 Immediate burial vs. above-ground

The following successional data are based on insects collected both through

exhumation and pitfall trapping At two weeks after death, the buried carcasses in both

28

Figure 9. Average linkage clustering of insect communities, based on the presence and absence of species collected from carcasses in the Coastal Western Hemlock (CWH) and Sub-boreal Spruce (SBS) biageoclimatic zones of British Cofumbia

CWH2uk-buried CWH2uk-delayed

CWH3mahow grd CWH 6 u k - h e d

, CWHM-delayed CWH 3mdelayed' CWH 6uk-above grd CWH3mbuned CwH 1 lmtxrrled CWH 16MFbuned

CWH 2uk-abve g d SBS2vk-above grd s 3 m t M l e d

/

S E h k - h e d - . S 6 C - W M

S6~k-bur led

W H 1 l m a l a e grd S B S l h M

zones were in the pnmary bloat stage (Table 2) I collected adults of s t e r a l spews

of b l o ~ d y (Calliphondae) from pitfall traps In both zones, but onl? (hllrphoru

vomrtoria (L ) and I,uc~/ra 11lristrr.s lanae In the SBS zone on buned carcasses (Table 1

4) Adults of the farmhes ?Iluscidae, Sphaerocendae, Phondae and Sarcophagdae

were collected from p~tfall traps above buned carcasses In both tones Adults and

pupae of fbrlrua canrirculurr.~ (L ) (Fanru~dae) were collected In the SBS zone on

buned carcasses and In p~tfall traps. but only adults uere collected In the CU'H zone at

t h s time 1 collected adult Staphyhn~dae. Sllphdae and Le~odtdae on buned carcasses

and In pitfall traps In both zones Lana1 Staph~lln~dae and Histendae *ere collected

In the SBS zone on buned carcasses h'mo,ira \lrtrrpenrrr\ (\Valker) (Pteromalldae)

and (brnpot~otus her~trlear~rrc (L ) (Formlc~dae) adults were collected on burled

carc&ses and in pitfall traps in both zones

The immediately buried carcasses were

~ . e e k s after death (Table 2 ) I collected pupae

(Calliphondae) and 0 p h j . r ~ lerrcosroma (R'ied

In the secondiq bloat stage bt st\

of &;-:rrculliphora lurr froni ( Hourrh L

) (hluscidae) from the ~mmediatet>

buried carcasses in the SBS zone (Table 4 ) Pupae of Hrdrotatw sp and . ifort~lltc~ sp

(Sluscidae) as well as lmae . pupae and adults of 1.: catrrrrcularr.~ were collected fiom

buried carcasses in both zones I)ohrtuphoro sp (Phondae) Imp were collected

fiom buried carcasses in the CNW zone I collected adults of these specres In ptrfdl /

traps above the buned carcasses at the same time

Tab

le 4

. co

ntin

ued.

C

WH

Zon

e S

BS

Zon

e

The buried carcasses did not reach the active decay stage until 3 months after ,

death, but the above-ground carcasses had reached this stage by 2 weeks after death . .

(Table 2). Phormia regirw and Protophormia ferraenovae (Robineau-Desvoidy)

imrnatures (Table 4) were found in large masses on the above-ground carcasses in

both zones L. illustrrs larvae and pupae were collected only from above-ground d

carcasses in the CWH zone, although adult L. illrrstris were collected fiom pitfall traps

a .

above buried pigs in the CWH zone and beside above-ground carcasses in the SBS

zone '~?ollected adult Hydrofaea sp , Leptocera sp (Sphaeroceridae), l>ohrrliphora

sp and bannia cam1culari.s in pitfall traps beside above-ground pigs in the SBS zone .,

Staphylinidae and Silphidae were'collected~froih above-ground carcasses and pitfall

traps in both zones I collected adult C'atqp ha.silarrs Say (Leiodidae) and larval

Staphylinidae fiom pitfall traps and above-ground carcasses in the CWH zone

I,eptocera sp , whose .pupal cases closely resemble those of the Piophilidae, ii

were collected as pupae on buried carcasses in both zones at 3 months after death,

during the active decay stage (Table 4) 1 collected Heleomyzidae larvae from buried

carcasses in the SBS zone 1 did mt observe maggot masses on any of the buried , '

carcasses in either zone

Buried carcasses in the CWH zone had entered advanced decay by I 1 months

after death and were still in t hs stage at 16 months after death (Tabl22) Buried

carcasses in the SBS zone were also in this stage when I exhumed !hem at 16 months

after death (Table 2) I collected very few insects on buried carrion at ths time

However, larval hsteridae were collected from buried carcasses at this point ( ~ i b l e a

4)

Above-ground carcasses in the CWH zone had entered the advanced decay

- stage by 6 weeks after death (Table 2) Adult Leptocera sp , Sphaerrdrum

hrprtst~~lafrrm ( F ) an8 Cterrrcera comes (Brown) (Elateridae) were collected from the

above-ground c8casses and pitfall traps, as well as adult and immature I.: cai.rnrcularrs

and Strnrrhra rlrgrrceps (Meigen) (Piophilidae) I also collected larval NecrophiI~~s sp. \

(Argyrtidae) from above-ground carcasses Since the above-ground carcasses in the .

SBS zone were eaten by a large scavenger, no hrther data were available

By 3 months after death, above-ground carcasses in the CWW zone had

entered the dryhemains stage (Table 2) Larval and adult I,epfoct.ra sp were collected

on the above-ground carcasses (Table 4) This was the first time that 1 collected lan.ae

of ttus species on above-goind carcasses Throughout the study. I observed theant

;I?crophoru.\ ~~wc.st~Kator Zetterstedt feeding on carcasses

2.5.2 Immediate vs. delayed burial

Immediately buried carcasses and cardasses buried 48 h after death all went

through the de~om~osl t~onal stages at the same rate, mth no measurable d~tferences

between the two treatments (Table 2 ) However, I obsened some d~flerences In Insect:

succession Although lilowflp adults tbf varrous spews r I

a b o ~ e carcasses tiom both treatments. I collected onh

on the delayed burial carcasses (Table 4) By 6 weeks after death I collected pupae of

the biou-fly species I;'. lar~fions and the muscid species 0. leucosroma from carcasses

buned 38 h after death, but not from immediately buried carcasses (Table 4). At 3

months after death 1 collected immature Heleomyzidae and Necrophilux sp f rom the

' \ ,

delayed burial but not the immediately buned carcasses (Table 4). The study of d

carcasses buried 48 h'after death was terminated at this point .

2.5.3 Immediate vs. disturbed burial

I observed differences in the presence of larval Calliphoridae and Muscidae

between the two treatments at 6 wk after death Pupae of the blowfly L. rllustrrs and

the muscids Hydrotuea sp , 0. leucostornu and Morelha sp were collected From the

undisturbed carcasses, but were not present on carcasses in the disturbed treatment ,

(Table 4) However, I collected pupae ofL. ~llus~rrs on these carcasses when they

were originally exhumed at 2 weeks after death (Table 4) Leprocera sp , Boerrcherra

sp (Sarcophagidae) and Neohellerra cooley (Parker) adults were collected in pitfall

traps above the undisturbed carcasses but not in pitfall traps above the disturbed

carcasses The Coleopteran family Histeridae was represented in both treatments with 1

Hrster drspuratar Say present on undisturbed carcasses and S. h~plrsrrrlarrrrn present

only on disturbed carcasses Larval Histeridae were present only on the undisturbed

carcasses (Table 4)

3. DISCUSSION

3.1 DIVERSITY IN EPHEMERAL HABITATS PI

Ephemeral habitats, such as carrion and dung are often very rich IQ species In

order for these insect species to survive. they must be mobile enough to colonize

empty habitats rapidly, in orde; to compensate for local population extinctions (Hanski

1987) The hgher species richness on buried than above-ground carrion (Figure 6) -7 .

contradicts the findings of Smith (1986) and Leclercq (1969) In contrast. the great&

evenness between species on buned than above-ground carnon is supported by other

authors (Leclercq 1969, Smith 1986)

Competition for resources could explain the lou d~versitv of Insect specles on

above-ground carcasses The carcasses were completely consumed. a frequent

occurrence for both camon and dung This has been observed to result in reductions

in lama], pupal and adult blowfly size (Hanski 1986. Hansk~ 1986) Coloruzat~on b)

tens or hundreds of species may occur (Payne 1965, Hansk~ 1986, .4nderson and

VanLaerhoven 1996) The predom~nance of Calllphorldae larvae on above-ground

carcasses (F lgre 7 ) suygests that competlt~on for resources b~ blouilc maggot masses

may have prevented other species fiom establ~shrng I t IS also possible that I rnlssed

collecttng some dlpteran species due to the o~erwhelm~ng abundance of'a feu spsctrj

w t h ~ n the maggot masses on aboke-ground carcasses (In burled carcasses. there

were no such maggot masses and little apparent competitiob by the few insects

present .

As postulated in the equilibrium theory of island biogeography (MacArthur and

Wilson 1972), species richness should be highest in large carrion habitats which are -

near other similar habitats and lowest in small, isolated habitats (Hanski 1987, #

~ewadikararn and Goff 1991) Because the carcasses in this study were all the same

size, burial of a carcass would have been equivalent to increasing the distance a

colonizing insect had to travel to reach it However, in contrast to the theory, the

species richness was greatest in the buried carcasses (Figure 7, Table 3), possibly due

to competition in the above-ground carcasses precluding the successfd colonization

by more species ,

Differences in species composition between the CWH and SBS zones (Figure

9) may reflect differences in the range of carrion-inhabiting species However, the

characteristics of the soil would also have influenced which species were present in the e

soil and available to colonize buried carcasses In addition, the physical characteristics A

of tbe soil after digging would determine which non-soil dwelling species could reach

the buried carrion (Kevan 1968) The presence of immature ('allrphor~~ vomrtorra and

I,~rc~lra rllustr~s on buried carcasses-at the two week exhumation in the SBS zone and

1,ucrlra ~llustris irknatures only on carcasses buried after 48 h in the CWH zone at the

same time period (Table 4) was likely due to differences in soil composition The soil

in the SBS zone sith was predominately clay which formed large coarse fragments

after excavation,' allowing easier access to the buried carcasses Calliphora and Lucrlra

spp (Table 4 ) (Fuller 1932) and species in the f$ly Phoridae (Lundt, 1964,

Nuorteva 19771, e g Dohrniphora sp (Table 4 ) are capable of burrowing (Lord el a1

1992) Nuorteva's ( 1977) statement that the presence of blowfly and Piophilidae

larvae on a buried body indicated that the body was kept unburied for a portion of &. time was evidently erroneous d

However, an alternative explanation-is also possible It rained during the

placement of carcasses in the CWH zone, preventing any fly acti.vity In the SBS zone,

it was warm and sunny during the 8 h it took to bury all the carcasses Some blowflies

could Have been attracted to the carcasses and oviposited before burial, but the -,

presence of younger instars still indicates that some penetrated the soil to reach the

carcasses

The-rapid development of insects on the above-ground carcasses during the

early stages of decay (Table 4) was undoubtedly influenced by action of maggot

masses ,which can increase the internal temperature of a carcass up to 40 "C, although I

this fluctuates considerably during a 24 h period (Anderson and VanLaerhoven 1996)

Because soil acts as a temperature sink, there was much less fluctuation in temperature

wittun the soil than in ambient air temperature (Figure 3) as also observed in other

studies, especially as depth within the soil increases (Kevan 1968, Wallwork 1970,

Wallwork 1976, Rodriguez and Bass 1985). The resulting consistently cooler

temperatures than in above-ground carcasses would have retarded the development of *

camon-inhabiting insects Any differential effects of low (CbT?) and fieezing (SBS) .

temperatures during the winter were not evident in ths study. despite a slight

difference in the rate of decomposition due to the winter soil conditions in the SBS

zone

The slower decomposition of buried than above-ground carcasses (Table 2 t

has also been observed in other studies (Lundt 1964, Pavne 1965, Payne et a1

1968) The rate .of decomposition of buried carcasses in both biorpeoclimatic zonm was

much slower than in South Carolina (Palme el a1 1968) The slow rate of

decomposition of buried camop explains the similarity of the cornrnuruties of insects

collected at 3 , 1 1 and 16 months after death in the CWH zone (Flpre 9) .tT

3.2 SUCCESSION

3.2.1 Immediately buried carcasses

3.2.1. I Dipteran carrion faun a a&

Numerous species of Diptera were predictably the most common inhabitants of - -

buned carcasses in ths study The collection of immature F i m m catuucu/a/i.t on

buried carcasses in both biogeoclhatic zones (Table 4 ) is consistent w i t h the common

occurrence of this ipecies in the soil (Peterson 1% 1 ), as well as on carrion in later

stagesaof succession (Anderson and VanLaerhoven 1996) Its early role in the

succession on buried camon is possibly due to the moisture associated wi th buned '*

carcasses, since ths species prefers moist hab~tat ,(Smith 1986)

I ')

/

The sequence in the SBS zone of (bllrphora vomrtorra larvae and pupae

during primary bloat (2 weeks after death), then HyJrotava sp , ~Morellia sp and

Ophy-a leucostoma pupae during secondary bloat (6 weeks after death) follows a

similar successional pattern to that found by Megnin ( 18941, who found a succession

of insects on buried carrion that began with C. vom~torra and Muscrna stahrrlarts soon

after death, followed by Ophyra.a)~thrm 0. lrucosloma were also collected from dog

cada~rers buried in coffins at 2 months after death in Washington, D C (Motter 1898)

In British Columbia, immature Hydrotaea sp were collected from 5 days to I0 months

after death on buried human bodies (Anderson 1995) Muscids have prewously been

collected from buried canion, but their time of colonization was not knonn (Lundt

1964, Nuorteva 1977) hly collection of hruohrllurru c t ~ ) l e , ~ (Sarcophagidae) adults

in pitfall traps above buried carcasses in the primary bloat stage. in the SBS zone 2

weeks after death agrees with the finding of thls species on buried human bodies 20

days after death in the Pnnce George Forest Region (Anderson 1995)

In the only experirnenta! study that used buried human cada~.ers, Calliphondae

and Sarcophagidae were collected from the cadavers but were identified only to the

family level (Rodriguez and Bass 1985) Other studies have been done on human &

bodies exhumed from actual homicide cases, or from anthropologcal studies (Mepin

1894, Motter 1898, Lundt 1964, filbert and Bass 1967, Leclercq 1969, Stafford

1971, Nuorteva 1977, Lord et a1 1992) The study by Rodriguez and Bass ( 1985)

utilued six cadavers each buried at a different time of year Unfortunately t h s ~ o r k

(Phondae) in pitfall traps above bloated bur;sd ;ar;ajw$ %r ?&-,:_.:- z _ -.s .--r

U recovery of larval Dohrnrphora sp from buned carcasses dunng 1;12i03:ljm b h : j r ,

the CWH zone and pupal of Leprocera sp from buried carcasses d u n n the act l ie e

stage in both zones (Tabie 4) agrees with the results of Payne (1968) who collected

adult I.tpr0~ rru sp and Ilohrrirphora rncr~rrralrs (Loew) dunng the bloat stage and

lamae of these two species at the onset of the active stage in Nonh ~ a r d i n a Motter

( 1898) stated that Phorldae colon~zed buried dog camon at 2 months after death, but

Megnin ( 1894) d ~ d not find f'hora a(tlrrrma on buried camon until a year after death

Nuorteva ( 1977) and Lundt ( 1964) noted the presence of Phoridae on buried bodies,

but did not indicate a time of colonization The occurrence of larval Heleomyzidae on

buried carcasses in the SBS zone during the active decay stage, at 3 months after

death (Table 4) is in agreement with Lundt's (1964) documentation of heleomyzids on

Staphylmdae bee1ie-s are cornmttnilt found on b u n d ;.ZZFF 6 LSZ- 4 7 -

Nuorteva 1977, Rodneez and Bass 1985 ) l n the t 'ancoti tc , Cw:kxf 3rd ? x z

Rupert Forest Reg~ons of Bnt~sh Columb:a- t anous species cf Srdphi trndac i kc*c

collected fiom buned human bod~es from 5 da:,s to 5 months aAw death ( It?-;fcrk.f-

1995) They were the predormnant beetles collected on buned camon In b o t h t*fltcs

throughout the 16 month period (Table 4 ) I found adult Yhrfrmthtttri sp at priman

bloat, much earlier than observed by Jle-gun (1894), u,ho stated that Yhrlttrtthrtt -

rhruirm did not arrive on buried bodies until two years af& death in France In b n h

Carolina. Staphylinidae were not present on buried pigs until the active stase (Pa?-ne tit

a1 1968), also later than in my study Other prominent beetles were the sdphjds

~l;rcrophoru.$ d<I;drem and ,.l..~crophond.$ rri\r.~rrgator (Table 4 ) 1 initially collec red

them fiom'buried carcasses dunng the primary bloat stage, in both zones These

results contradict a pre\rious report that silphds could not locate camon buned under

4 cm of sand (Shubeck 1985)

3.2.1.3 Hjmenopteran carrion faun a

The carpenter ant ('amponortc.\ herctrlt>am.c- was the.most common

hymenopteran 1 collected I t occurred dunng the primaq bloat stage., on bumd "

carcasses in both biogeoclirnatic zones (Table 4 ) In North Carolma, P a p e 31 uf

f 1%8) collected other ant species dunng the fiesh and bloat stages From a pig carcass -

in a simulated coffin Perpetrators rarely bury homicide victims in coffins and this . -

scenario would influence the ability of insects to reach the carcass. ':

3.2.2 Carcasses buried after 48 hours

I t has often been assumed that the presence of blowfly larvae, pupae or pupal

cases indicates that a body has remained above ground for a period of time prior to #

burial (Gilbert and Bass 1967, Nuorteva 1977, Vanezis et a1 1978, Heath 1982)

This assuriiption is contradicted by published evidence (Lord el a/ 1992). as well as

data fiom this study (Table 4) Nuorteva (1977) stated that the presence of Histendae

indicated that the body was left unburied for at least 2-3 days and that the presence of

Piophlidae indicated that the body was left unburied for at least a week However I

collected Hrster drspuraror adults and hlsterid larvae from immediately buried

carcasses in the SBS zone I did not collect piophllid larvae from immediately buried

carcasses, but adults were caught in pitfall traps above immediately buried carcasses in \

' the SBS zone, implying that they were attracted to the buried remains It is possible

that immature Piophilidae larvae were not collected fiom buned carcasses in this

experiment due to the conversion of fatty tissue into adipocere, removing the favored

food of Piophlidae (Smith 1986) Thus, none of my results can be used to indicate

conclusively whether or not delayed burial has occurred

L

3.2.3 Disturbed burial

Slrnilarly, there was no evidence that exhumation and re-burial allowed

, colonization by species not typically found on buried carcasses or that it gave species

. that weie incapable of penetrating 30 cm of soil a chance to reach a buned carcass

ow ever; my study is hampered by small sample size In the LTni;ted States, times of

disturbance as well as elapsed time since death have been determined using insect

evidence (Anderson pers com ) Since th s effect is likely to be site spetlfic, ir is

important to be aware of this possibility More research is required to determine under

what ecological conditions t h s effect may be obsewed

3.3 Ecological Roles of Carrion Fauna

During heterotrophc succession, entomophagous insects tend to increase as

the smcession continues (Mohr 1943, Payne 1965) The most common predators in t

. - the soil are beetles in the families Carabidae and Staphylinjdae (Kevan 1968, ,?>

Wallwork 1976) Although the great majority of insects collected in this study were

saprophagous, generalist predatory carabid, histerid and staphylinid beetles, as well as

ants and wasps were well represented on both above-ground and buried carcasses in

both zones, probably feeding on dipteran eggs and larvae I, also collected elaterid

beetles but this family has both carnivorous and saprophytic members (Kevan 1968,

Wallwork 1976) Predaceous dipteran larvae, Ophyra 1euco.stomu and Hvdrortrtw sp

were collected on buried carcasses. the former In the SBS zone and the latter In both

3.4. t Elapsed Time Since Desrtb

The major'use of forensic entomoiogy has been to determine elapsed time since

death The elapsed time s m e death can be used to confirm or refute a suspect's alibi

and to a d in the identificat~on of unknown kictims by focusing an investigation into the

correct time frame Ths information can be vital in a homicide investigation #

(.i\nderson and t'anlaerhoven 1996) . -

There are two methods of determining elapsed time since death using insect

ekldence (Goff 1903) The first uses maggot age and developmental rates Since

blouflies usually arrive and begin laying eggs within minutes after death (Anderson

and VanLaerhoven l996), an analysis of the oldest insects present will give a

minimum post-mortem interval This requires accurate colkction of the oldest insects

and accurate temperature records The second method uses the suc~ess~on of msects

on a decompos~ng corpse An entomolnglst can pred~ct a w + i n d o ~ of t ~ m e In whrch

death occurrexl b\ analvzlny the presence and absence of specw on a hod\ 4lthouyh

and b e e r r biogmfimattc zones in 8 C . indicating that databases for particular

zones and ~cenafio~ must be estabfisheh before entomological evidence can be used ,

-' accurately

3.4.2 Temperature f

In the case of a crime scene, the temperature ofthe body prior to discover).

must be predict4. i~ order to determine the minimum post-mortem interval using

maggot developmental rates This js usually done by comparing temperature data -*

taken at the scene, wifh data from the nearest weather station during the same time -

, period If there isfa good correlatiori between the two, then the weather station data .~ -77 wr ' . I

, r - l % @ . *

can be used to predict - what the temperature at theTscenk was prior to'diskovery of th; L -

body This technique assumes that there is a good correlation between-the ambient .' - . *, * I 1

temperature at the scene and the interna?aemperature of the body In my study, there -a .

- ..* .-

a' 1 *

was a poor correlation between fh6weather station ambient$@ tempeiature a id the . '4 * -

intehal temperature of above-ground carcasseS in the CWH zone (Table P), probably, - 1 due to maggot mass acti;ty raising the internal carcass temperature &d for a

. . I I

1 . 3 . . 1

micrometeorological differences betwken the weatlikr stationand the research sites . c

Suppo.rt fdr th'ese causeb are faund'in the kxcelltmt conetation between ambient air and '? 1 / - *

- . d

internal above-sound carcass temperature in the SQS z6& (~abl; I ) befirelnaggot 4

. . s

mass activity raised the internal carcass temperature and when the two temperatures . ' , 7

+ s .

8 . - - - P were recorded within 1 m,of each other Since ther;wer& no rqaggotAmasses on any -, =

of the buried bodies, it is not surprising that ambient air temperature wakwell' .= or - ::I

so I 1

I .

1 h

4

conelated (Table I ) w t h internal buried carcass temperature, at least during the

spnng. summer and fall in the SBS zone During the winter in the SBS zone, ambient

air temperature continued to fluctuate, but internal temperature of the buried carcass in

the frozen ground did not, resulting in no correlation (Table 1) t

Because soil temperature was the best predictor of internal buried carcass

temperature (Table l), it wouldbe best to establish soil temperatures at scenes of

buried victims The strong relationship between soil and weather station temperat&es

in the CNV zone (Table 1 ) indicates that soil temperature can be correlated with - .

1

weather station temperature data after discovery of a'buried cadaver Soil temp'erature

has been used in at least one case, to determine blowfly development rates (Lord er al *

3.4.3 indicator species .

T& occurrence of certain species of insects on buried carcasses at predictable . ,

tlmes In thg succession suggests that these sspecles can be used as rndicators of the

elapsed time since death.of a buried homrclde victim -

The de\elopmental rates of cailiphond flies are known for a variety of . 9 j

4 ;empeiatures (fiuoneba 1977, Greenberg 1993) m a h g them extremely useful -'

indicators of the post-mortem interval Third instar lanae of { 'ulhphoru vomrlcvru and H -

-

- 5 .=

I rrc~l,$ r l l~~\ l r r \ uerc present bv t h e evhurnation at 2 weeks after death m the SBS B

zone Using the soil temperature and the stage of development. it is possible to ' * .-

e

determine how long it took these flies to reach third instar, whch was the oldest stage %

collected at 2 weeks after death Using Greenberg's developmental data for ('

vornltorla at 12 5•‹C (1993), death occured on or before 15 June 1997 Using

Nuorteva's developmental data for L. rllustris at 15•‹C (1977), death occurad on or4

before 16 June 1997 Because both these estimates use a temperature higher than was L

actually found ar the scene (mean internal buried carcass temperature of 11 6"C), death

must have occured earlier than 15 June 1997 Thls is aaconservative estimate be~ause k h "

e

this assumes that the larvae had just entered third instar, when in actuality, they likely

had been in that stage for a few days The actual date o f death was'10 June 1997

In the C W zone, prepupal I, rllusrrts were collected from carcasses buried $3 I

L

hours after death Using the soil temperature and the stage.of development, l t is j

- ,

possible to determine how ldng it took these fLes to reach stage. w h ~ h

was the oldest stage collected at 2 weeks after death Using . f * uoneva's developmental

data for /*. iNir.ctr1.c jlt I 5'C ( 1977). death occured on or before 2 1 June 1997 , .

Because this estimate uses a temperatu-re higher than was actually found at the scene r

(mean Internal buried carcass temperature qf 1-2 2•‹C) . death must have occured earller

than 21 June 1997 Thls IS a consekatlve-estlmate because this assumes that the larvae *

I

C

pal, wbeii in actuality, thev could had been In that stage for a

.of death was I?:Jun_e 1997 0

3.4.3.2 Family Muscidae w

\ X' r

The family Muscidae contains some potential indicator species that could be

used to calculate the elapsed time since death. At 6 weeks after death, pupal

Hydrotaea sp, and Morelha sp were collected fiom buried carcasses in both zones,

and pipal Ophyra leucosloma were collected fiom buried carcasses in the SBS zone

(Table 4) If the developmental rates for these three muscids were known at particular

temperatures, the time taken for irnmatures to reach the pupal stage could be

calculated, thus giving a minimum post-mortem interval

3.4.3.3 Family Fan n iidae

Fanniid'hies are usually considered to colonize cadavers late in the succession

of insect species However, pupal I.a)~ma ca~~rtrcrrlarls were collected from buried

carcasses at 2 weeks after death in the SBS z a e and larval and pupal F: cantlrctrlarrs

were collected tiom buried carcasses at 6 weeks after &ath in the CWH zone, possibly

due to the wet condition of the buried carcasses whch is preferred by members of this

family Therefore, when using this species to predict a minimum post-mortem internal,

it is important to note its early arrival on buried earrion, as well as the difference in

arrival tirnes between the two zones

3.4.J.4 Family Ph oridae

Larvae of Dohrn~phora sp were collected on buried carcasses in the CWH

zone at 6 weeks after death The presence of immatutes of t h s species gives a

minimum post-mortem interval of > 2 weeks after death and < 6 weeks after death

3.4.3.5 Family Sph aertxeridae

Pupae of l q r c m r a sp were collected on buried carcasses in both zones at 3 2

months after death The presence of immatures of th s species gives a minimum post-

mortem interval of > 6 weeks after death and < 3 months after death Pupal'cases of

l,t~ptoct.ra sp were collected on buried carcasses In the CWH zone at 1 1 months after

death The presence of pupal cases of this species gives a minimum post-mortem

- interval of . 3 months and < 1 1 months after death

3.4.3.6 Familr. Helermyzidae

Lawae of'this family were collected on buried carcasses in the SBS zone and

on carcasses burled after 48 hours In the CWH zone at 3 months after death (Table 4 )

Th~s f a m ~ l ~ I S also a later success~onal specles, s~nce the presence of mrnatures gibes a

mlnlmum post-mortem intewal between 6 weeks and 3 monfhs after death

3.4: 3. 7 C'oleopreran Families

Since most of the coleopteran spec~es~collected on the burled carcasses are

general predators, they cannot be used to determ~ne a post-mortem intenal

t 1. When using the succession of insect species to determine the elapsed time since

death of a buried hdmicide victim, it is important to have a database of insect

succession for that particular ecosystem Therefore ideally, a successional C

database for each maj,or biogeoclimatic zone should be established

2. Since dipteran species other than those tiom the family Calliphoridae could be used

as indicator species, more studies on the developmental rates of these species

uould alloh the estimation of a more preclse post-mortem interval

3.- When using the developmental rates of early successional dipteran species to

f

determme the elapsed t~me since death of a buried homicide victim, a datalogger

should be placed in the soil for comparison to the nearest weather station If the

weatffer statlon records soil temperature, th~s should be used rnstead of ambient air

temperature

4. Since disturbance can potentially change the succession of insect species on a

buried homrclde victim. more research should be done to determine under what

ecological conditions this effect may arise and how to determine when this

disturbance has. occurred

5. Although depth of burial was not examined in ahis study, it probably affects the

succession of Insect species on the carcasses Therefore. more research should be

done to determine how the depth of burial influences insect succession ,

6. Because no maggot masses were observed on any buried carcass, the presence of

maggot masses, large numbers of b l o q y pupae or blowfly pupal cases on a buried

' -* homicide victim is a probable indicator that the body was not buried immediately

Ths is a possible indication that the crime scene and the death scene are not the . .

same, therefore investigators should deteimine where the body was after death. but

pior to burial *

4. REFERENCES JI.

' - Anderson, G S. Assistant Profess or, School ology, Simon Fraser University, Burnaby , B C , personal communication

I

Anderson, G S 1995 The use of insects in death investigations an analysis of, forensic entomology in British Columbia over a five year p e ~ o d Can Soc. Forensic Sci J 28 (4) 277-292

Anderson, G S and S L VanLaerhoven 1996 Initial studieson insect succession on carrion in southwestefn British Columbia J Forensic Sci. 4 1 (4) 6 17-625 '

Catts, E P and M L Goff 1992 Forensic entomology in criminal investigations Ann Rev Entomol 37 253-272

Denno, R F and w R Cothran 1976 Competitive interaction and ecological '

strategies of sarcophagid and calliphorid flies inhabiting rabbit carrion Ann Entomol Sot: Am 69 109-1 13 . -,

. Dillon, L C 1997 Insect succession on carrion in 3 biogeoclimatic zones of B C- Dept of Biological Sciences, Simon Fraser uru*vers& M Sc thesis

Dillon, L C and G S Anderson 1995 Forensic Entomoiogy f he use of insects in death investigations to determine elapsed time since-death Cana ian P o k e Research Centre Rep No TR-05-95 f

a

Fuller, M E 1932 The effect of carcass burial on blowflies J Coun Sci Ind Res 5 162- I64

. Grlbert, B M and U' M Bass 1.967 Seasonal dating of b u d s fiom the presence of fly pupae Am Antiquity 32 534-535

Goddard, J and P' K Lago 1985 Notes on blow-f?y (Diptera Calliphoridae) succesion on carrion in Northern Mississippi J Entomol Sci 20 3 12-3 17

Goff, M L 1991 Comparison of insect species associated with decomposing remains'

P recovered inside dwellings and outdoors on the island of Oahu, Hawaii J Forensic Sci 36 748-753

Goff, M L 1993 Estimation of Postmortem interval using arthropod development and successional patterns Forensic Sci Rev 5 8 1-94

Goff. XI L and M M Hym 199 1 Detemnation of postmortem ~ntewal b! arthropod succession a case study fiom the H a ~ a l a n islands J Forensic Sci 36 607-614 '

Goff. !bl L and C B Odom 1987 Forens~c entomology in the Hawallan Islands. L' S A Three case studies Am J Foren bled Path 8 45-50

Goff, M L , C B Odum and M Early 1986 Estimation of postmortem intenal by entomological t echques a caw study fiom Oahu, Hatvat Bull Soc L'eaor ECOI 1 1 242-236

Goff, X I L , A 1 Omon and K Gunatilake 1988 Estimation of postmortem intenal by arthropod succession Three case studies fiom the Hauattan islands .b J Foren Sled Path 9 220-225

Greenberg, B 1993 Different developmental strateyies in t u o boreal blou flies (Diptera Calllphondae) J hfed Entomol 3 (2 ) 481-484

Greenberg, B 1985 Forens~c entomolop case studies Bull Enromol Sof .Am 3 1 (4 ) 25-28

Hanski. I 1987 Colonization of ephemeral habitats, 1.V Coiomzatlon. successton and stability .A J Gray era/ . Ed Bntlsh Ecoloyical Soclet!. &fo;d pp 155- l8b

Hanski, 1 1986 Nutnt~onal ecolog of dung- and c a n o n - f d t n y inserts . I.$' hutritional ecology of insects, nut=. spiders and related intenebratrs F Slansky and J G Rodriguez Ed John Wile\,. Xeti 't'wk pp 53?-835

Heath, A C G 1982 Beneficial aspects of b l o ~ flies hew Zedand Enromol 7 (.; I 333-338

Heuadikaram. K and ?.I Goff 199 i Effect of carcass size on rate of decomposrtton and arthropod succession patremj .9m J For >fed Path 12 2 3 S - Z W

Ke~an , D K 31 1968 Soil arumals H F &: G m'itherby, London

Krebs. C J 1989 Ecologcal msthodoiop Harper &: Row, \eu l'or'h

Leclercq. 31 1969 Entomolglcal parasitoiog, entornolop and legal medicine Pergamon Press. &ford

Lord. ti' D . T R Xdhns and E P Carts 1992 The use of .$r-rtrh?tirmrit f?a&fiti~ ( I ' m Der U'ulp (Dlptera 3lusadae I and (biilphora 1 1 6 IIW ( ~obineau- Dest*oid!) (Dipiera Calllphondae) to estimate the tlme of death of a bod\ buned under a house I . 4 p c Enforno1 9 ( 4 ) 22 ' -235

+-rh2 )d ; Ezostlegcd obsen at runs a b u t the invaslon of msect s into carcasses ttuned tn s o i l Pedobiologia 4 158

%lac Arthur, R H and E 0 Wilson 1972 The theory of island biogeography Princeton University Press, Princeton, N J

M e p n , P 1894 Faune des cadavres application de I' entomologie a la medicine legale Encyclopedik Sci h d e - Memoire, Paris . .

hjeidinyer, D and J Pojar 1991 Ecosystems of British Columbia British Columbia Ministry of Forqts

Micrbsoft 1985 Microsoft Excel, 5 0 Microsoft Corporation

Minitab 1994 10 I Minitab Inc , 308 1 Enterprise Drive, State College, PA 1680 1 - 3 008

Mohr, C 0 1943 Cattle droppings as ecological units Ecol Monogr 13 275-309

Motter, M G 1898 A contribution to the study of the fauna of the grave - a study of 150 disinterments, with some additional observations J N Y Entomol Soc 6 201-23-31

d Nuorte\a, P 1977 Sarcosaprophagous Insects as forensic ind~cators. IN Forensic medtc~ne a study In trauma and enwonmental hazards C G Tedeschl Ed Saunders, Neu York pp 1072- 1095

Paye , J A 1965 .4 summer carrion study of the baby pig Sirs Scrt!Jb L Ecology 46 592-602 .

. .

P a y e , J A , E U' K~ng and G Be~nhart 1968 Arthropod succession and decompos~tnon of buned p~gs Nature 2 19 1 180- 1 18 1

Peterson, A 1951 Larvae of insects s > - Part I1 Lithoprint Edwards, Ann Arbor. * Mlchlgan C

% t ,

~ e e d : H R 1958 A study of dog carcass communities in Tennessee wth special reference to the ~nsects Am Mmd Nat 59 2 13-245

1

Rodriguez, W C and W ' M Bass 198b Decompositioniof buried bodles and methods that may aid in their lo&tfon' F , 1' Forensic Sci 30 836-852

b

Shubeck, P P 1985 Orientation of carrion beetles to camon buned irndcr s;.=r. lavers of sand (Coleoptera Silphdae) Entomol \eu s 96 15;- ' +**

Sk~nner, M and R A Lazenby 1983 Found! Human Remains Archeology Press, Simon Fraser University, Burnaby, B C

Smith, K G V 1986 A manual of forensic entomology British Musern (Nat Hist ) London, and Cornell University Press Ithaca, N Y

Spitz, W U and R S Fisher. 1973. Medicolegal investigation of death Charles C Thomas, Springfield, Illinois

Stafford, F 197 1 Insects of a medieval burial Sci and Anth 7 6- I0

Vanezls, P , B G Sims and J H Grant 197-8 Medical and scientific investigations of an exhumation in unhallowed ground Med Sci Law 18 209-22 1

s

Wallwork, J A 1976 The distribution and diverstiy of soil fauna Academic Press, New York

Wallwork, J A 1970 Ecologlr of soil animals McGraw-Hill, London